An evo-devo geek's scientific meanderings

insects

Hah, I open my Google Reader (damn you, Google, why do you have to kill it??? >_<), expecting to find maybe a handful of new articles since my last login, and instead getting both Nature and Science in one big heap of awesome. The latest from the Big Two are quite a treat!

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By now, of course, the internet is abuzz with the news of all those four-winged birdies from China (Zheng et al., 2013). I’m a sucker for anything with feathers anywhere, plus these guys are telling us in no uncertain terms that four-wingedness is not just some weird dromaeosaur/troodontid quirk but an important stage in bird evolution. Super-cool.

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Then there is that Cambrian acorn worm from the good old Burgess Shale (Caron et al., 2013). It’s described to be like modern acorn worms in most respects, except it apparently lived in a tube. Living in tubes is something that pterobranchs, a poorly known group related to acorn worms do today. The Burgess Shale fossils (along with previous molecular data) suggest that pterobranchs, which are tiny, tentacled creatures living in colonies, are descendants rather than cousins of the larger, tentacle-less and solitary acorn worms. This has all kinds of implications for all kinds of common ancestors…

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Third, a group used a protein from silica-based sponge skeletons to create unusually bendy calcareous rods (Natalio et al., 2013). Calcite, the mineral that makes up limestone, is not normally known for its flexibility, but the sponge protein helps tiny crystals of it assemble into a structure that bends rather than breaks. Biominerals would just be ordinary rocks without the organic stuff in them, and this is a beautiful demonstration of what those organic molecules are capable of!

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And finally, Japanese biologists think they know where the extra wings of ancient insects went (Ohde et al., 2013). Today, most winged insects have two pairs of wings, one pair on the second thoracic segment and another on the third. But closer to their origin, they had wing-like outgrowths all the way down the thorax and abdomen. Ohde et al. propose that these wing homologues didn’t just disappear – they were instead modified into other structures. Their screwing with Hox gene activity in mealworm beetles transformed some of the parts on normally wingless segments into somewhat messed up wings. What’s more, the normal development of the same bits resembles that of wings and relies on some of the same master genes. It’s a lot like bithorax mutant flies with four wings (normal flies only have two, the hindwings being replaced by balancing organs), except no modern insect has wings where these victims of genetic wizardry grew them. The team encourage people to start looking for remnants of lost wings in other insects…

Or how I learned (again) that there are no truly simple stories in biology.

In the name of fairness and plain old intellectual integrity, I should mention some interesting new developments in the treehopper-helmet-novelty issue. Back in the first treehopper post I acknowledged that I’m a far cry from an entomologist, and a new study argues that Benjamin Prud’homme and the entire crew on Prud’homme et al. (2011) may share that attribute with me.

A paper published recently in the open-access online journal PLoS ONE (Mikó et al., 2012) questions basically every interpretation the previous study made about those funky thoracic appendages. After dissecting, CT-ing and microscoping several treehoppers and related insects, they conclude that:

The helmet is not an appendage that articulates with the first thoracic segment – it’s actually most of the first thoracic segment itself.

The joint at the base of the helmet is the articulation between the first two thoracic segments.

The paired “helmet buds” Prud’homme et al. reported are more likely to be artefacts of the way they sectioned their specimens, since Mikó et al. couldn’t find any in treehoppers of a similar developmental stage.

If all of this is correct, that would suggest that the helmet has nothing to do with wings, it’s just like other less extreme outgrowths of the thorax that you find in a large variety of insects.

What about the genes?

If you take a gander at the first treehopper post or Prud’homme et al. (2011) itself, you’ll see that they supported their microscopic observations with gene expression data including two appendage-specific genes and one that they considered specific to wings. However, even I had a note of caution about using Dll/Dlx genes – which seem to be there whenever anything starts sticking out of an animal’s body – as evidence of homology to anything. Mikó et al. (2012) point out that nubbin, the supposed “wing gene” actually has quite variable roles in wing and other appendage development when you look at more insect species besides fruit flies. The Hth-Dll combo, it appears, is also involved in the development of more obviously non-wing thoracic outgrowths, like beetle horns.

Where does that leave us?

Seeing as I’m still no entomologist, I can’t really take sides in the anatomical arguments. The genetics? What immediately springs to my mind is Keys et al. (1999), and how some butterflies grow their eyespots by the wholesale co-option of a genetic regulatory circuit from wing development. Did the same sort of thing happen to beetles and treehoppers, then?

This, in fact, only reinforces my general opinion about novelties and the nature of genetic evidence. Evolution rarely, if ever, works from scratch, and the boundary between “novelty” and “tinkering” is as blurry as it gets. Thus, “homology” is rarely a clear-cut and straightforward issue. All of that still stands [1], even if treehoppers might have shifted on some sliding scales. (Which direction is an interesting question. Is a re-activated wing homologue more or less “novel” than a generic thoracic outgrowth patterned by some wing circuitry? Does the distinction even make sense?)

All in all, this is getting quite interesting. It feels decidedly like the beginning of a heated debate [2]. I’ll certainly keep an eye out for future episodes of the treehopper saga.

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[1] Though I have to say, I have a couple of papers on my reading list that may mess with my opinions… Don’t want to jinx it, so I won’t say more, but I’m hoping to make a post out of them one day.

This is a quickie to share something randomly fascinating, courtesy of Schnakenberg et al. (2011). Their study looked at the effect of killing a certain cell type in the sperm storage organs of female fruit flies. They mainly looked at the effect of this on things like, well, sperm storage, sperm behaviour, number of eggs the females laid.

Experimental flies weren’t as good at laying eggs as normal females, and the reason for this is the really interesting bit. The eggs were fully formed and by all accounts, normal – they just got stuck inside the mother. And kept developing, to the point where the researchers could coax nearly-hatched eggs with wriggling maggots inside from the females.

I can’t go all “ha! this is how live birth evolves!” at creationists, since none of these maggots were actually born without the experimenters messing with their mothers. Still, that’s the sort of surprise I would like to see when I do creepy things to innocent little animals!

Apparently, those extravagant shapes are all due to one special body part called the helmet – an outgrowth of the first thoracic segment of these insects. (Here‘s a little reminder of insect anatomy.) It only occurs in treehoppers, according to Prud’homme et al. (2011). I confess, I know very little about insects in general, and nothing about treehoppers in particular, but talk of evolutionary novelties always gives me a little kick.

[NOTE: I won’t define “novelty” exactly. You can probably figure out what it means, and it’s one of those funny concepts that defies an easy definition. Which is kind of the point of this post, though I didn’t originally intend it to come out that way.]

Evolutionary novelty, at least in complex, multicellular organisms like animals, is usually thought to come from tinkering more than “true” innovation. This is thought to hold on all levels; new genes are often modified versions of old genes, new cell types originate from old cell types, and new body parts are built on old body parts. If you think about it, this makes perfect sense: the old parts are already there, doing jobs that can be used as a starting point, whereas sticking a mutation in a piece of DNA that doesn’t encode anything and stumbling on a useful new gene is not exactly the likeliest event in evolution.

[ASIDE: Whole new body parts practically have to come from old parts on some level – the probability of evolution assembling a complex organ entirely from scratch has many times more zeroes after the decimal point than the probability of accidentally making a new gene. The question is how much of the new part is new. Is it built almost completely from an old structure, such as a whole arm – individual bones, muscles and everything – being modified into a wing, or does it only borrow basic building blocks and put them together in a completely new way?]

The outlandish helmets of treehoppers (sort of) uphold the prevailing view. Prud’homme et al. (2011) tell us that this has been a matter of some controversy – most held that they were “true” novelties that were not homologous to any other body part, but there were clues that there’s more to the story than that. And, indeed.

The first hints were anatomical. Helmets don’t simply grow out of the animal’s back – they are attached by a joint. Above that, they share a few other details, including their tissue structure and their veins, with the appendages almost all insects bear on their other thoracic segments: wings. What’s more, although the mature helmet is a single structure, it develops from two precursors that eventually fuse together. Two wings, two helmet primordia, you get the picture.

Prud’homme et al.‘s investigation involved more than dismantling the thoraxes of baby treehoppers. Homologous structures often share a common genetic underpinning, so they checked the expression of some “wingy” genes (or, to be precise, their protein products) to see just how deep the similarity between helmets and wings extended. The first of these, Nubbin, is wing-specific in better-studied insects. As expected if helmets are homologous to wings, the developing helmet was chock full of Nubbin. The two other genes they analysed, Distal-less (Dll) and homothorax (hth), are more generally expressed in insect appendages (wings, legs and antennae), defining their different regions from base (hth) to tip (Dll). They showed the same expression pattern in the helmet – which doesn’t necessarily mean that helmets are modified wings, but it does suggest they are based on some kind of appendage. And, given what appendages the other thoracic segments bear in the same position…

[NOTE: Well, I don’t know much about hth, but Dll is a bit problematic in this respect. It’s not just an “appendage gene” in insects, but also in a wide variety of other animals. Were it not for Dll expression, no one would suggest homology between, say, the tube feet of a starfish and the legs of a fly (Panganiban et al., 1997) – it’s pretty likely that Dll was originally more of an “anything that sticks out of the body” gene than an “appendage”, never mind a “wing”, gene proper. Dll/Dlx genes also do other stuff, like making neurons migrate in vertebrate brains (Anderson et al., 1997). So Dll expression alone doesn’t mean something is an appendage, let alone a specific type of appendage. Luckily, it’s not alone here. Incidentally, this is lesson number one of comparative/evolutionary developmental genetics. When the question is homology of a structure or process, always look at combinations of genes.]

This is not too surprising given the evolutionary history of wings, or what the fossil record was kind enough to preserve for posterity. The first known winged insects (link leads to drawing of Stenodictya lobata in Grimaldi and Engel, 2005) actually had winglets on the first thoracic segment as well, but those were lost before the last common ancestor of living insects. (How that happened in genetic terms, and how it may have been reversed in treehoppers, is also discussed in the paper, but it isn’t directly relevant to the novelty issue) In a way, treehoppers’ “invention” is a giant laugh in the face of Dollo’s Law, which proposes that complex features don’t re-evolve once they are lost (I kind of touched on this “law” here).

Nevertheless, helmets look nothing like wings and function nothing like wings. (To be fair, they look nothing like one another, either.) They are so dissimilar to their proposed evolutionary sisters that apparently their relationship eluded most researchers. How “novel” are they, then? It’s something of a philosophical question. Since, at this level of complexity, literally nothing comes from scratch, at what point do we stop calling something “tinkering” and start calling it “true novelty”?

As with most philosophical questions, I don’t think this one has a correct answer. That doesn’t mean these questions are not worth pondering. The way we word things influences the way we think about them. Exactly where (or even if) we draw a line between two fuzzy concepts isn’t important in my opinion. But to be aware that there is a dilemma about that line, and that other people may draw it in different places, is. Effective communication is one of my Big Issues, and being critical of your own thinking is an issue that ought to be Big for anyone doing science. (Or for anyone, full stop.) Thinking about unanswerable questions like this is a great way of exercising those (self-)critical muscles.

(Originally, I just wanted to gush about the excitement of figuring out the origin of novelties, but I managed to turn it into a philosophical treatise. Whoda thunk that? <.< )